Neonatal immunity associated with heterologous HIV-1 neutralizing antibody induction in SHIV-infected Rhesus Macaques

Sommer Holmes, Hui Li, Xiaoying Shen, Mitchell Martin, Ryan Tuck, Yue Chen, Elena E. Giorgi, Hélène Fradin Kirshner, Madison Berry, Elizabeth Italie, Sravani Venkatayogi, Joshua S. Martin Beem, Robert J. Edwards, Katayoun Mansouri, Ajay Singh, Cindy Kuykendall, Thaddeus Gurley, M. Anthony Moody, Nicole DeNayer, Todd Demarco, Thomas N. Denny, Yunfei Wang, Tyler D. Evangelous, John T. Clinton, Bhavna Hora, Kshitij Wagh, Michael S. Seaman, Kevin O. Saunders, Nicholas Solomotis, Johnathan Misamore, Mark G. Lewis, Kevin Wiehe, David C. Montefiori, George M. Shaw and Wilton B. Williams ()
Additional contact information
Sommer Holmes: Duke University School of Medicine
Hui Li: University of Pennsylvania
Xiaoying Shen: Duke University School of Medicine
Mitchell Martin: Duke University School of Medicine
Ryan Tuck: Duke University School of Medicine
Yue Chen: Duke University School of Medicine
Elena E. Giorgi: Fred Hutchinson Cancer Center
Hélène Fradin Kirshner: Duke University School of Medicine
Madison Berry: Duke University School of Medicine
Elizabeth Italie: Duke University School of Medicine
Sravani Venkatayogi: Duke University School of Medicine
Joshua S. Martin Beem: Duke University School of Medicine
Robert J. Edwards: Duke University School of Medicine
Katayoun Mansouri: Duke University School of Medicine
Ajay Singh: University of Pennsylvania
Cindy Kuykendall: Duke University School of Medicine
Thaddeus Gurley: Duke University School of Medicine
M. Anthony Moody: Duke University School of Medicine
Nicole DeNayer: Duke University School of Medicine
Todd Demarco: Duke University School of Medicine
Thomas N. Denny: Duke University School of Medicine
Yunfei Wang: Duke University School of Medicine
Tyler D. Evangelous: Duke University School of Medicine
John T. Clinton: Duke University School of Medicine
Bhavna Hora: Duke University School of Medicine
Kshitij Wagh: Los Alamos National Laboratory
Michael S. Seaman: Harvard Medical School
Kevin O. Saunders: Duke University School of Medicine
Nicholas Solomotis: BIOQUAL Inc.
Johnathan Misamore: BIOQUAL Inc.
Mark G. Lewis: BIOQUAL Inc.
Kevin Wiehe: Duke University School of Medicine
David C. Montefiori: Duke University School of Medicine
George M. Shaw: University of Pennsylvania
Wilton B. Williams: Duke University School of Medicine

Nature Communications, 2024, vol. 15, issue 1, 1-23

Abstract: Abstract The details of the pediatric immune system that supports induction of antibodies capable of neutralizing geographically-diverse or heterologous HIV-1 is currently unclear. Here we explore the pediatric immune environment in neonatal macaque undergoing Simian-HIV infection. Simian-HIV infection of 11 pairs of therapy-naive dams and infant rhesus macaques for 24 months results in heterologous HIV-1 neutralizing antibodies in 64% of young macaques compared to 18% of adult macaques. Heterologous HIV-1 neutralizing antibodies emerge by 12 months post-infection in young macaques, in association with lower expression of immunosuppressive genes, fewer germinal center CD4 + T regulatory cells, and a lower ratio of CD4 + T follicular regulatory to helper cells. Antibodies from peripheral blood B cells in two young macaques following SHIV infection neutralize 13% of 119 heterologous HIV-1 strains and map to regions of canonical broadly neutralizing antibody epitopes on the envelope surface protein. Here we show that pediatric immunity to SHIV infection in a macaque model may inform vaccine strategies to induce effective HIV-1 neutralizing antibodies in infants and children prior to viral exposure.

Date: 2024
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DOI: 10.1038/s41467-024-54753-6

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